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Infection and Immunity, June 2006, p. 3251-3261, Vol. 74, No. 6
0019-9567/06/$08.00+0     doi:10.1128/IAI.00245-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Environmental Signals Generate a Differential and Coordinated Expression of the Heme Receptor Gene Family of Bartonella quintana

James M. Battisti, Kate N. Sappington, Laura S. Smitherman, Nermi L. Parrow, and Michael F. Minnick*

Division of Biological Sciences, The University of Montana, Missoula, Montana 59812

Received 14 February 2006/ Returned for modification 10 March 2006/ Accepted 17 March 2006

Of all bacteria, Bartonella quintana has the highest reported in vitro hemin requirement, yet an explanation for this remains elusive. To produce diseases such as trench fever, endocarditis, and bacillary angiomatosis, B. quintana must survive and replicate in the disparate environments of the Pediculus humanus corporis (body louse) gut and the human vasculature. We previously identified a five-member family of hemin binding proteins (Hbps) synthesized by B. quintana that bind hemin on the outer surface but share no similarity to known bacterial heme receptors. In the present study, we examine the transcription, regulation, and synthesis of this virulence factor family by cultivation of the bacterium in environments that simulate natural heme, oxygen, and temperature conditions encountered in the host and insect vector. First, quantitative real-time PCR data show that hbpC expression is regulated by temperature, where a >100-fold increase in transcript quantity was seen at 30°C relative to 37°C, suggesting that HbpC synthesis would be greatest in the cooler temperature of the louse. Second, cultivation at human bloodstream oxygen concentration (5% relative to 21% atmospheric) significantly decreases the transcript quantity of all hbp genes, indicating that expression is influenced by O2 and/or reactive oxygen species. Third, a differential expression pattern within the hbp family is revealed when B. quintana is grown in a range of hemin concentrations: subgroup I (hbpC and hbpB) predominates in a simulated louse environment (high heme), and subgroup II (hbpA, hbpD, and hbpE) is preferentially expressed in a simulated human background (low heme). By using two-dimensional sodium dodecyl sulfate-polyacrylamide gel electrophoresis, immunoblotting, and matrix-assisted laser desorption ionization—time of flight mass spectrometry fingerprinting, we demonstrate that synthesis of HbpA correlates with hbpA transcript increases observed at low hemin concentrations. Finally, an hbpA promoter-lacZ reporter construct in B. quintana demonstrates that a transcriptional regulator(s) is controlling the expression of hbpA through a cis-acting regulatory element located in the hbpA promoter region.

* Corresponding author. Mailing address: Division of Biological Sciences, The University of Montana, Missoula, MT 59812. Phone: (406) 243-5792. Fax: (406) 243-4184. E-mail: mike.minnick{at}mso.umt.edu.

Editor: D. L. Burns

Infection and Immunity, June 2006, p. 3251-3261, Vol. 74, No. 6
0019-9567/06/$08.00+0     doi:10.1128/IAI.00245-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Parrow, N. L., Abbott, J., Lockwood, A. R., Battisti, J. M., Minnick, M. F. (2009). Function, Regulation, and Transcriptional Organization of the Hemin Utilization Locus of Bartonella quintana. Infect. Immun. 77: 307-316 [Abstract] [Full Text]  
  • Battisti, J. M., Smitherman, L. S., Sappington, K. N., Parrow, N. L., Raghavan, R., Minnick, M. F. (2007). Transcriptional Regulation of the Heme Binding Protein Gene Family of Bartonella quintana Is Accomplished by a Novel Promoter Element and Iron Response Regulator. Infect. Immun. 75: 4373-4385 [Abstract] [Full Text]  
  • Boonjakuakul, J. K., Gerns, H. L., Chen, Y.-T., Hicks, L. D., Minnick, M. F., Dixon, S. E., Hall, S. C., Koehler, J. E. (2007). Proteomic and Immunoblot Analyses of Bartonella quintana Total Membrane Proteins Identify Antigens Recognized by Sera from Infected Patients. Infect. Immun. 75: 2548-2561 [Abstract] [Full Text]  


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